Loss of NF-κB activation in Kupffer cell-depleted mice impairs liver regeneration after partial hepatectomy

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 292, Issue 6, 2007, Pages

  Abshagen, Kerstin ^a   Eipel, Christian ^a   Kalff, Jörg C ^b   Menger, Michael D ^c   Vollmar, Brigitte ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

Author keywords

Clodronate; Hepatocytes; In vivo fluorescence microscopy; Interleukin 6; Nuclear factor b; Proliferating cell nuclear antigen; Tumor necrosis factor

Indexed keywords

CLODRONIC ACID; CYCLIN B1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOSOME; TUMOR NECROSIS FACTOR ALPHA; BISPHOSPHONIC ACID DERIVATIVE; CYCLIN B; CYCLINE; LE CL2MDP; LE-CL2MDP; METHANE; RELA PROTEIN, MOUSE; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA BINDING; FEMALE; FLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; KUPFFER CELL; LIVER PARENCHYMA; LIVER REGENERATION; LIVER WEIGHT; MOUSE; MOUSE STRAIN; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; STATISTICAL SIGNIFICANCE; WESTERN BLOTTING; ACTIVE TRANSPORT; ANIMAL; BLOOD; DRUG EFFECT; LIVER; LIVER CELL; LIVER RESECTION; METABOLISM; ORGAN SIZE; PARACRINE SIGNALING; PATHOLOGY; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; TIME;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL PROLIFERATION; CYCLIN B; DIPHOSPHONATES; HEPATECTOMY; HEPATOCYTES; INTERLEUKIN-6; KUPFFER CELLS; LIVER; LIVER REGENERATION; METHANE; MICE; MODELS, ANIMAL; ORGAN SIZE; PARACRINE COMMUNICATION; PROLIFERATING CELL NUCLEAR ANTIGEN; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 34447558580     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00399.2006     Document Type: Article

References (43)

1. Abshagen K, Eipel C, Menger MD, Vollmar B. Comprehensive analysis of the regenerating mouse liver: an in vivo fluorescence microscopic and immunohistological study. J Surg Res 134: 354-362, 2006.
2. Akerman P, Cote P, Yang SQ, McClain C, Nelson S, Bagby GJ, Diehl AM. Antibodies to tumor necrosis factor-α inhibit liver regeneration after partial hepatectomy. Am J Physiol Gastrointest Liver Physiol 263: G579-G585, 1992.
3. Aldeguer X, Debonera F, Shaked A, Krasinkas AM, Gelman AE, Que X, Zamir GA, Hiroyasu S, Kovalovich KK, Taub R, Olthoff KM. Interleukin-6 from intrahepatic cells of bone marrow origin is required for normal murine liver regeneration. Hepatology 35: 40-48, 2002.
4. Assy N, Minuk GY. Liver regeneration: methods for monitoring and their applications. J Hepatol 26: 945-952, 1997.
5. Assy N, Gong Y, Zhang M, Pettigrew NM, Pashniak D, Minuk GY. Use of proliferating cell nuclear antigen as a marker of liver regeneration after partial hepatectomy in rats. J Lab Clin Med 131: 251-256, 1998.
6. Black D, Bird MA, Hayden M, Schrum LW, Lange P, Samson C, Hatano E, Rippe RA, Brenner DA, Behrns KE. TNF-α-induced hepatocyte apoptosis is associated with alterations of the cell cycle and decreased stem loop binding protein. Surgery 135: 619-628, 2004.
7. Boulton RA, Alison MR, Golding M, Selden C, Hodgson HJ. Augmentation of the early phase of liver regeneration after 70% partial hepatectomy in rats following selective Kupffer cell depletion. J Hepatol 29: 271-280, 1998.
8. Chaisson ML, Brooling JT, Ladiges W, Tsai S, Fausto N. Hepatocyte-specific inhibition of NF-κB leads to apoptosis after TNF treatment, but not after partial hepatectomy. J Clin Invest 110: 193-202, 2002.
9. DeAngelis RA, Markiewski MM, Taub R, Lambris JD. A high-fat diet impairs liver regeneration in C57BL/6 mice through overexpression of the NF-κB inhibitor, IκBα. Hepatology 42: 1148-1157, 2005.
10. Decker K. Biologically active products of stimulated liver macrophages (Kupffer cells). Eur J Biochem 192: 245-261, 1990.
11. Dietrich DR. Toxicological and pathological applications of proliferating cell nuclear antigen (PCNA), a novel endogenous marker for cell proliferation. Crit Rev Toxicol 23: 77-109, 1993.
12. Ding H, Peng R, Reed E, Li QQ. Effects of Kupffer cell inhibition on liver function and hepatocellular activity in mice. Int J Mol Med 12: 549-557, 2003.
13. Eipel C, Schuett H, Glawe C, Bordel R, Menger MD, Vollmar B. Pifithrin-α induced p53 inhibition does not affect liver regeneration after partial hepatectomy in mice. J Hepatol 43: 829-835, 2005.
14. Fausto N. Liver regeneration. J Hepatol 32: 19-31, 2000.
15. FitzGerald MJ, Webber EM, Donovan JR, Fausto N. Rapid DNA binding by nuclear factor κB in hepatocytes at the start of liver regeneration. Cell Growth Differ 6: 417-427, 1995.
16. Fujita J, Marino MW, Wada H, Jungbluth AA, Mackrell PJ, Rivadeneira DE, Stapleton PP, Daly JM. Effect of TNF gene depletion on liver regeneration after partial hepatectomy in mice. Surgery 129: 48-54, 2001.
17. Greene AK, Puder M. Partial hepatectomy in the mouse: technique and perioperative management. J Invest Surg 16: 99-102, 2003.
18. Hayashi H, Nagaki M, Imose M, Osawa Y, Kimura K, Takai S, Imao M, Naiki T, Kato T, Moriwaki H. Normal liver regeneration and liver cell apoptosis after partial hepatectomy in tumor necrosis factor-α-deficient mice. Liver Int 25: 162-170, 2005.
19. Iimuro Y, Nishiura T, Hellerbrand C, Behrns KE, Schoonhoven R, Grisham JW, Brenner DA. NFκB prevents apoptosis and liver dysfunction during liver regeneration. J Clin Invest 101: 802-811, 1998.
20. Karin M, Yamamoto Y, Wang QM. The IKK NF-κB system: a treasure trove for drug development. Nat Rev Drug Discov 3: 17-26, 2004.
21. Kinoshita M, Uchida T, Nakashima H, Ono S, Seki S, Hiraide H. Opposite effects of enhanced tumor necrosis factor-α production from Kupffer cells by gadolinium chloride on liver injury/mortality in endotoxemia of normal and partially hepatectomized mice. Shock 23: 65-72, 2005.
22. Kirillova I, Chaisson M, Fausto N. Tumor necrosis factor induces DNA replication in hepatic cells through nuclear factor κB activation. Cell Growth Differ 10: 819-828, 1999.
23. Laurent S, Horsmans Y, Stärkel P, Leclercq I, Sempoux, Lambotte L. Disrupted NF-κB activation after partial hepatectomy does not impair hepatocyte proliferation in rats. World J Gastroenterol 11: 7345-7350, 2005.
24. Lazar G. The reticuloendothelial blocking effect of rare earth metals in rats. J Reticuloendothel Soc 13: 231-237, 1979.
25. Lee CM, Yeoh GC, Olynyk JK. Differential effects of gadolinium chloride on Kupffer cells in vivo and in vitro. Int J Biochem Cell Biol 36: 481-488, 2004.
26. 2MDP-liposomes alters hepatic cytokine expression and delays liver regeneration after partial hepatectomy. Liver 20: 66-77, 2000.
27. Michalopoulos GK, DeFrances MC. Liver regeneration. Science 276: 60-66, 1997.
28. Naito M, Hasegawa G, Ebe Y, Yamamoto T. Differentiation and function of Kupffer cells. Med Electron Microsc 37: 16-28, 2004.
29. Naito M, Nagai H, Kawano S, Umezu H, Zhu H, Moriyama H, Yamamoto T, Takatsuka H, Takei Y. Liposome-encapsulated dichloromethylene diphosphonate induces macrophage apoptosis in vivo and in vitro. J Leukoc Biol 3: 337-344, 1996.
30. Orfila C, Lepert JC, Alric L, Carrera G, Beraud M, Pipy B. Immunohistochemical distribution of activated nuclear factor κB and peroxisome proliferator-activated receptors in carbon tetrachloride-induced chronic liver injury in rats. Histochem Cell Biol 123: 585-593, 2005.
31. Rai RM, Loffreda S, Karp CL, Yang SQ, Lin HZ, Diehl AM. Kupffer cell depletion abolishes induction of interleukin-10 and permits sustained overexpression of tumor necrosis factor α messenger RNA in the regenerating rat liver. Hepatology 25: 889-895, 1997.
32. Seki E, Tsutsui H, Iimuro Y, Naka T, Son G, Akira S, Kishimoto T, Nakanishi K, Fujimoto J. Contribution of Toll-like receptor/myeloid differentiation factor 88 signaling to murine liver regeneration. Hepatology 41: 443-450, 2005.
33. Shiratori Y, Hongo S, Hikiba Y, Ohmura K, Nagura T, Okano K, Kamii K, Tanaka T, Komatsu Y, Ochiai T, Tsubouchi H, Omata M. Role of macrophages in regeneration of liver. Dig Dis Sci 10: 1939-1946, 1996.
34. Su AI, Guidotti LG, Pezacki JP, Chisari FV, Schultz PG. Gene expression during the priming phase of liver regeneration after partial hepatectomy in mice. Proc Natl Acad Sci USA 17: 11181-11186, 2002.
35. Takeishi T, Hirano K, Kobayashi T, Hasegawa G, Hatakeyama K, Naito M. The role of Kupffer cells in liver regeneration. Arch Histol Cytol 62: 413-422, 1999.
36. Van Rooijen N, Sanders A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 174: 83-93, 1994.
37. Van Rooijen N. The liposome-mediated macrophage "suicide" technique. J Immunol Methods 124: 1-6, 1989.
38. Vollmar B, Glasz J, Post S, Menger MD. Depressed phagocytic activity of Kupffer cells after warm ischemia-reperfusion of the liver. J Hepatol 20: 301-304, 1994.
39. Vollmar B, Rüttinger D, Wanner GA, Leiderer R, Menger MD. Modulation of Kupffer cell activity by gadolinium chloride in endotoxemic rats. Shock 6: 434-441, 1996.
40. Wolf F, Wandke C, Isenberg N, Geley S. Dose-dependent effects of stable cyclin B1 on progression through mitosis in human cells. EMBO J 25: 2802-2813, 2006.
41. Yamada Y, Kirillova I, Peschon JJ, Fausto N. Initiation of liver growth by tumor necrosis factor: deficient liver regeneration in mice lacking type 1 tumor necrosis factor receptor. Proc Natl Acad Sci USA 94: 1441-1446, 1997.
42. Yang l, Magness ST, Bataler R, Rippe RA, Brenner DA. NF-κB activation in Kupffer cells after partial hepatectomy. Am J Physiol Gastrointest Liver Physiol 289: G530-G538, 2005.
43. Yu L, Sun ZJ, Wu SL, Pan CE. Effect of resveratrol on cell cycle proteins in murine transplantable liver cancer. World J Gastroenterol 9: 2341-2343, 2003.